POSTNOTE

Number 619 March 2020 UK Decline and Extinctions

Overview ◼ There have been documented declines in insect species and populations. Generalist species are less likely to decline than more specialised species. The impacts of this on ecological processes are poorly quantified. ◼ The UK has unparalleled data from long- term monitoring, but it is limited by gaps in what is measured and how. There are few long-term data sets with abundance data. provide vital goods and services for ◼ Drivers of decline, such as habitat loss, are wildlife, food production and human health, common across insect groups and can and their decline threatens important natural interact to cause combined pressure on processes. Despite some insects being in long- populations. However, environmental term decline, a few species are showing stable changes can benefit some species while or increasing trends. Insects can respond to negatively affecting others. interventions quickly. This POSTnote will ◼ Interventions, such as habitat creation, may summarise the evidence for insect declines in play a role in halting declines, but the scale the UK, the drivers of trends, and interventions and types need careful consideration. to support the recovery of insect populations.

Background Limitations of UK Insect Decline Data Insects play a pivotal role in natural processes that support An ideal dataset for understanding insect decline would include other living organisms, and human health and well-being insects from a wide range of ecosystems, using samples (POSTnote 281). Adult insects have six legs and usually one or collected in a standardised way.3,39,40,20,33 Globally, data on two pairs of wings and are the most diverse group of .1– 4 Roles include pollination (POSTnote 348 and 442), pest and Box 1: Economic Importance of Beneficial Insects weed regulation, decomposition, nutrient cycling, and provision Insects have economic, social and cultural value.2,9,41–43 A of food for wildlife and humans (Box 1). They can also be decline in insects may negatively impact ecosystem services,44,45 and could be costly.46 Currently, there is limited agricultural pests or transmit disease (Box 2).5–18 Insects are evidence for the quantitative value of ecosystem services 9,19,20 key indicators for monitoring ecosystems (POSTnote 312). provided by insects, but some examples are emerging. The economic value of pollination to UK crop production is Concerns about insect decline attracted wider attention approximately £500 million a year.47,48 Dung beetles are following studies showing large declines in insect abundance estimated to be saving the UK cattle industry £367 million and biomass.21–23 Recent media attention has claimed each year and £37.42 per cow through reducing flies and 49 unprecedented declines in insects across the globe leading to increasing nutrients in the soil. Natural pest control (by ground beetles and parasitoid wasps) of widespread aphid an ‘insectageddon’24 causing the “collapse of nature”.25 These pests is worth up to £2.3 million per year in South East claims were largely based on a review of scientific articles from England wheat fields alone.46,50 Freshwater insects in their across the globe.26 However, this study has been criticised as larval stage, such as dragonflies or mayflies, can also filter the evidence it reviewed was predominantly from North water, remove pollutants and provide food for bats17, birds51 52 America and Europe, which may have skewed the conclusions. and fish (such as salmon and trout ). This supports It also excluded studies that reported stable or increasing recreational activities, including angling (which contributed £1.46 billion to the English economy in 201553). Insects also populations by only selecting those showing a decline.27–31 As have social and cultural value.54 Some studies have such, the trends for global insect populations remain largely attempted to quantify the value the public place on insects; unknown but could be underestimated.32,33 However, studies in for example, a study found that people were willing to pay Europe found insect abundance or biomass declined between approximately £43 per household per year to support bee 55 38% and 75%.21,34–38 protection policy; equating to £842 million per year when scaled up to 31 million taxpayers.

The Parliamentary Office of Science and Technology, Westminster, London SW1A 0AA 02072192840 [email protected] parliament.uk/post @POST_UK

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insects are limited because of the large number of species.1,3,56 mammals, plants and insects (4–8%).19 However, a study found The UK has more data than many countries due to its long-term that butterfly distribution declined more than birds and plants.34 recording schemes, natural history collections, citizen science engagement and insect research community.57,58 Emerging Declines in abundance or distribution have been seen in bees 32,101 34 35 102 labour-efficient methods can help data collection through and hoverflies, butterflies and moths, beetles, and 48,101,103,104 remotely monitoring larger areas, such as bioacoustics59–62 and freshwater insects. However, some species are 105 BioDAR63–65 (see POSTbrief 36).66 New identification methods increasing in biomass. The data available for the most such as DNA analysis may prove more reliable in the future studied insect groups are summarised below. 67–74 (see POSTbrief 36). New methods still require expert Bees and Hoverflies interpretation. Current data are limited by gaps in what is Bees and hoverflies experienced dramatic losses between the measured and how, including:3,40 1950s and 1980s but losses have slowed since the 1990s.77 Of ◼ Methods. Surveys that used a standardised sampling across 353 wild pollinator species, 117 (33%) had decreasing sites, measured at systematic intervals, exist for a limited distributions (1980–2013).32 Yet, 10% of species had increasing group of species and habitats.40,75–78 distributions.3297 The rest (57%) had an unclear trend.32 ◼ Time. Limited data are available before the 1970s,79 creating Pollinators key to European crops increased by 12%, potentially an arbitrary baseline for comparison.40,80 Using data collected supported by agri-environment schemes or the increased area irregularly across time may lead to uncertainty.56,81,82,33 of oilseed rape.32,106,107 Since 1909, 20 bee and wasp species ◼ Location. The gaps in where data are collected can lead to have gone extinct in Britain.108 a bias towards some habitats such as nature reserves and agricultural systems. The trends from these systems may not Butterflies and Moths be transferable to other systems. This bias has begun to be Of 62 butterfly species, 19 (31%) are threatened and four have 40,76,81,82 addressed through several schemes. gone extinct in GB.109 Butterfly abundance has declined for 21 ◼ What is measured. Data focus on specific insect groups; species since 1976.110 However, abundance increased for 11 such as bees,83 rather than other groups, such as species111 (such as silver-washed fritillary with a 127% decomposers;2,3,56,84 and more easily observed adult forms increase).112 Of 337 moth species, 111 (33%) had increasing rather than caterpillars or aquatic larvae.66 trends but 222 (66%) were declining, and 71 species declined ◼ The type of data can affect the conclusions made about by over 30% per decade (1968–2004).100 Total GB moth insect declines. For example, species richness tells us the abundance has decreased by 31% (1969-2016).100,113Moth number of species present. However, abundance (number of declines occurred in coastal, urban and woodland habiats.113 individuals of a species) may have a stronger link with However, some evidence suggests that moth biomass may be ecosystem services than richness.9,21,45,85–87 Without knowing increasing, implying that a few species are doing well.79 the abundance and species identity, changes in communities can be masked.88 The range of data can make comparisons Beetles 98 across insect groups, locations and time difficult but Of 1134 beetle species in GB, 13% are threatened. A statistical modelling can be used.85,89 significant decline in abundance of ground beetles was found in ◼ Who is collecting data. The reliance on volunteers means 75% of 68 species, and 34 of those species decreased by 30% 102 that there is often irregular sampling.39,85,90 To continue each decade (1994–2008). The number of species also collecting data, long-term investment into resources, building declined.102 However, abundance in chalk downlands, skills and capacity, is required to sustain volunteers, support woodlands and hedgerows increased (16–57%).102 amateurs and incentivise professional development.40,91–97 ◼ Accessing data. Some data are fragmented (held privately Box 2: Pests and Invasive Non-Native Species by researchers, or companies like agricultural or While other insects are in decline, there are concerns that 101 environmental consultancies, see POSTbrief 36).40 pest species (native and invasive) such as weevils, aphids,112 and cabbage stem flea beetles110 may be Trends in UK Insects increasing (POSTnotes 303, 394, 439), with negative impacts on crop yields.114,115 Climate change and emerging resistance The UK has experienced extinctions and declines in abundance, of pests to insecticides116 amplifies this increase117 biomass and distribution of insects. Of the 2430 GB insect (POSTnote 597). Although some invasive species can create species assessed by Natural England, 55 have gone extinct and opportunities (such as increased pollen availability), others 286 (11%) are threatened.98 Total aerial insect biomass pose risks (such as increased predation, see POSTbrief 118 declined at one of four sites since 1973.99 Data from 3089 36). The impact of the invasive species depends on the abundance and the role it plays in the system. For example, insect species showed that the distribution size for terrestrial some invasive plants are readily taken up by native insects increased during 1970–1980s but declined sharply pollinators but these interactions are poorly understood and between 2005–2015.83 However, freshwater insects have risks could be overlooked with limited knowledge.118 Invasive recovered since the early 2000s.83 Insects have also become predators tend to exert strong top-down pressure on less widely distributed by 10% on average (1970–2015).19 insects.44,119,120 For example, the Asian hornet feeds on bees.47 Other stressors, such as disease and pesticides, can Insects may be declining faster than other groups.100 The make bees more vulnerable to predation.121,122 Risk registers average abundance of insect indicator species (butterflies and include non-native species with potential economic risks, but are less effective at capturing the ecological risks.123 moths) is decreasing while bird and mammal abundance remains stable.19 Declines in distribution are comparable across

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Freshwater Insects Box 3: Commercially Used Insect Population Trends Of 724 aquatic insect species in GB, 68 (9%) are threatened Bumblebees and solitary bees are managed but little is and 11 have gone extinct.98 A recent UK study found that known about these populations in the UK as registration is dragon-fly, caddis-fly and mayfly distributions decreased in the not required.47 Current evidence is biased towards pollinators 167 1970–1990s, but recovered in the 2000s to above 1970 such as honey bees. Honey bee colonies and bee-keepers decreased by 31% across Europe between 1985–2005.133 levels.101 Species with increasing distributions tend to be However, registered honey bee colonies in the UK grew from 124 generalists or have adapted to warmer climates. A study in 90,000 in 2008 to 247,000 in 2017.185 These figures may be Wales found that populations of specialist caddis-flies, stone- inaccurate as honey bee registration is voluntary.47 The flies and beetles were more likely to decline even if overall drivers of honey bee declines are most likely economic, such as difficulty in making money from bee farming, the reduced species richness remained stable.88 cost of importing bees,133,186 and high costs of treating diseases and concern over pesticide exposure.186–188 Diseases Drivers of Insect Trends can contribute to declining numbers47,189 although the scale There are a variety of drivers behind insect decline and their of impact on recent declines remains unclear (see POSTbrief impacts differ across habitat, species and time (see POSTbrief 36).133 The management of disease relies on good bee- 36). There is a lack of evidence on how some of these drivers keeping practice.47,190 There is limited knowledge on how 47,167,191 affect different insects as the impacts may have already disease impacts services or wild insects. Managed bees (honey191,192 and bumble193) share pathogens with wild occurred prior to sufficient monitoring.40,99,126,127,33 Drivers may pollinators, with potential for negative impacts (bumblebees, also interact with each other and increase their impact on insect solitary bees or hoverflies) but the direction in which the populations.41,47,128,129 For example, bees can be more infection occurs is unclear.191,193-196 Managed bees can also susceptible to parasites and the effects of habitat loss during compete with wild pollinators for resources. exposure to pesticides.128,130 Climate change is likely to interact with multiple stressors such as habitat loss.35,37,131,132 Wild and The impacts of this combined exposure remain unclear.47 commercially-managed insects share drivers of decline such as These chemicals can build up in soils and plants, and can run loss of habitats, reduced variety in plants and exposure to off into water systems, further impacting insects.12,197–199 chemicals (Box 3).128,133–135 Key drivers are known to include: There is limited evidence on the impacts of pesticides on ◼ Habitat loss, fragmentation and degradation. Habitat non-target insects that aren’t pollinators; with most research loss and degradation caused by land-use change can reduce since 2014 focussing on the impacts of neonicotinoid the resources for insects across their life stages (breeding pesticides (Box 4).167 sites, foraging sites, shelter from weather and ◼ Climate change can affect individual insect species both predators).47,66,136,137 Hostile environments between positively and negatively.19,35,84,125,162,200–209 For example, due fragmented semi-natural habitats make it more difficult for to a warming climate, aphids had an earlier and longer flight species to move (POSTnote 300).138 Specialist species are season and were able to reproduce more compared to more vulnerable to the impacts of land-use change.47,108 For previous years; becoming more abundant.112,200 Changes in example, some species are reliant on human-modified weather and temperature can alter the timings of insect habitats, such as brownfield sites.139 lifecycles that can negatively impact fitness or prevent ◼ Urbanisation can impact habitat connectivity.128 Pollution, emergence altogether.89,112,158,210–215 Of 130 butterfly and including air, water and light, can impact insects but moth species, 39 had increasing abundance, but early evidence on these is limited (see POSTbrief 36).140–151 Some emergence led to neutral or negative impacts for 91 urban habitats, such as gardens, can support high and species.216 The range of some species has expanded unique insect biodiversity but are often dominated by northwards and upwards while others have contracted.84,131 generalist species.152–160 These changes in communities can lead to temporary ◼ Land-use intensification. Large-scale monoculture is often increases in the number of species through the rise of novel accompanied by high chemical inputs, tillage and mowing.161 ecosystems.217 This can impact insects through habitat loss, degradation and fragmentation.23,47,162 Although monoculture of some Box 4: Neonicotinoid Pesticides crops provides resources for pollinators,47 the simplification In 2018, an EU-wide ban was applied due to poisoning and 163 44 of the landscape can reduce plants and nesting sites. sublethal effects on pollinators44 (which can translate to Crops only flower for a short time, whereas wildflowers offer reduced reproduction or colony level failures)218 but evidence resources throughout insect lifecycles.41,44,136,164 This can for other insects is limited (Commons Briefing Papers 219–224 contribute to decreased insect abundance, and changes in SN06656). However, risk of exposure remains, with 222 223 community composition and ecosystem service persistent detectable levels and increased toxicity across environments.171 Honey bees and bumble-bees can exhibit provision.44,45,134,165,166 preferences for neonicotinoid-treated food over time, making ◼ Pesticides, fertilizers and veterinary medicines. it difficult to control their exposure.224 Neonicotinoids can Chemicals are used in rural and urban environments that can also negatively impact aquatic systems.14,172,225,226 In have unintended direct and indirect negative impacts on non- response to the ban, older and less effective insecticides are target wildlife,14 including insects.47,107,135,162,167–184 In one being used, as are newer insecticides that have limited evidence of impact.47,227–230 study of wild pollinator individuals with detectable levels of chemicals, 71% had been exposed to more than one compound.168 This increases toxicity and stress.12,169,170

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Interventions to Support Insect Recovery Box 5: Urban Habitat Creation The Wildlife and Countryside Act 1981 prevents collecting or Urban spaces; such as brownfield sites, ponds, road/rail killing of a small number of butterfly, moth and beetle verges, gardens, allotments and green roofs; support species.231,232 The Natural Environment and Rural Communities insects.153,155–160,254,262–267 Reducing mowing can support 268,269 Act 2006 identifies individual insect species for conservation.233 insects but appropriate timings should be explored. Flower mixes should be chosen carefully to support The Habitats Directive (92/43/EEC) covers seven UK insect pollinators and provide breeding habitat.136,160,270–272 234 species. The 2014 National Pollinator Strategy is being However, public perception may pose a barrier to delivered with a range of stakeholders. Future policy implementation. There is a concern that road or rail suggestions for insect recovery have been published.235,20 interventions could create an ‘ecological trap’ by drawing Future policy for England includes commitments set out in the pollinators to dangerous areas, exposing them to risks from 273 25-Year Environment Plan for the Natural Environment.236 This cars and pollution. Another option is reducing the use of pesticides in urban areas.47,168,171,274–276 Bee or bug ‘hotel’ includes creating or restoring 500,000 hectares of wildlife-rich effectiveness depends on the quality of the surrounding habitat outside protected sites as part of a Nature Recovery habitat.47,277 Light pollution may also limit effectiveness.135 Network to connect habitats across the country.237 This enables ‘Re-wilding’ gardens can reduce chemicals and increase insects to move through habitats, allowing some species to habitats such as flowers and ponds.278–282 Rewilding could adapt to changes in climate. The Environment Bill 2019-2020 also restore processes on a larger scale (POSTnote 537). makes provisions for setting long-term biodiversity targets.238 acres and common species.283–287 Training land managers can Insect conservation can support other animals and demonstrate improve the quality of implementation.288–290 For example, the quality of the environment.9,19 Insects have the potential to appropriate tree planting that creates diverse habitats can recover faster than other groups due to their rapid life support insects,291–296 but planting appropriate native trees cycles and can even respond to small scale interventions (see supports more insect species than introduced tree species.297 Box 5). Evidence synthesis of measures to address the drivers of decline is skewed towards pollinators, but new studies are Other Interventions for Agricultural Land 239 addressing this. Other interventions can include organic farming,17,47,298 diversifying crops,41,44,47 beetle banks,299 and reducing inputs Habitat Creation, Connection and Protection (fertilizers, herbicides, pesticides and fungicides,251 or livestock Protecting and creating habitats for other groups (plants or medical treatments12,41,197). Freshwater insects benefit from birds) can support insects,240–242 but more targeted buffer strips that decrease run-off pollution in freshwater conservation for insects would include conserving a range of systems.300 Training and education around chemical use can habitats (semi-natural and micro).47,243–248,20 For example, prevent and reduce impacts.44 However, bans can also be heathlands can protect important pollinator-plant effective in reducing the use of high-risk chemicals (Box 4).44 interactions.240,249 Wild pollinators250,251 are supported by bare ground (for nests),250 flower strips,106,136,252,253 restored grass Integrated Pest Management gives preference to non-chemical and heathland,249,250,254 and nest boxes and uncropped naturally methods to manage pests such as using crop rotations, field regenerated field margins.32,251 Chalk and limestone grassland, margins and biological control.47,236,301–303 In 2017, the National broadleaved woodland, and natural grassland produce the Farmers Union developed a self-assessment tool for farmers.304 greatest amount of nectar per unit area.136 This has been completed by 16,820 farmers and growers, covering 25% of the UK total agricultural area.47 However, this The success of habitat creation is determined by its structure, data are not public so there is no current review being resources (such as nectar, dung or food plants), the extent of undertaken on the effects, at a farm-scale, on insects.47 fragmentation and diversity of surrounding habitats, and the absence of pressures (POSTbrief 34).10,47,66,106,255,256,20 For Box 6: Reintroductions and Assisted Colonisation example, hedgerows in a landscape can act as corridors to Reintroducing species to habitats they naturally occupied or 156,257,258 facilitate insect movement. Habitat creation can be to habitats with continued climate suitability can reverse implemented in either urban areas (Box 5) or agricultural land. extinctions and increase complexity and resilience of Species that have become locally extinct can be re-introduced systems.45,305,306 For example, two UK butterfly species to protected or created habitat (Box 6). (marbled white and small skipper) were introduced to sites in Northern England that were outside of their existing range Habitat Creation on Agricultural Land but had a suitable climate. Both populations grew and Under the Agriculture Bill 2019-20, results-based payments expanded their range.305 This is called assisted 305 could be made to incentivise high-quality implementation that colonisation. Reintroductions that are evidence-based and supported by stakeholders are more likely to be successful. maximises the complexity and connectivity of habitats An example is the large blue butterfly, which is of global 259 (POSTNote 377). This could be supported by co-operative importance but was extinct in the UK in 1979 and incentives that encourage peer-to-peer knowledge exchange reintroduced in the 1980s.307 It became very abundant at a and working at a larger scale. The evidence on the uptake and number of sites by 2014308 and benefited other species309 quality of implementation is limited.260 For example, flower (some endangered307). Understanding the large blue’s mixes and hedgerows may have increased since 2015 because relationship with a species of red ant and the wider ecosystem was essential for successful reintroduction. of the Countryside Stewardship Scheme package,47,261 but it only represents 1% of national nectar provision.136 The benefits of these interventions are limited to a few surrounding Endnotes:

POST is an office of both Houses of Parliament, charged with providing independent and balanced analysis of policy issues that have a basis in science and technology. POST is grateful to Rebecca Robertson for researching this briefing, to the BES for funding her parliamentary fellowship, and to all contributors and reviewers. For further information on this subject, please contact the co-author, Dr Jonathan Wentworth. Parliamentary Copyright 2020. Image copyright © CC BY-SA2.0 gailhampshire POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 5

1. Collen, B. et al. (2012). Spineless: status and trends 20. Samways, M. J. et al. (2020). Solutions for humanity of the world’s invertebrates. on how to conserve insects. Biological Conservation, 2. Noriega, J. A. et al. (2018). Research trends in Vol 242, 108427 ecosystem services provided by insects. Basic and 21. Hallmann, C. A. et al. (2017). More than 75 percent Applied Ecology, Vol 26, 8–23. decline over 27 years in total flying insect biomass in 3. Cardoso, P. et al. (2019). Predicting a global insect protected areas. PLOS ONE, Vol 12, e0185809. apocalypse: Insect apocalypse. Insect Conservation 22. Lister, B. C. et al. (2018). Climate-driven declines in and Diversity, Vol 12, 263–267. abundance restructure a rainforest food 4. “Insect.” The Merriam-Webster.com Dictionary. web. Proceedings of the National Academy of Merriam-Webster Inc. Sciences, Vol 115, E10397–E10406. 5. Kleijn, D. et al. (2015). Delivery of crop pollination 23. Seibold, S. et al. (2019). Arthropod decline in services is an insufficient argument for wild pollinator grasslands and forests is associated with landscape- conservation. Nature Communications, Vol 6, 7414. level drivers. Nature, Vol 574, 671–674. 6. Phillips, B. B. et al. (2018). Shared traits make flies 24. Monbiot, G. (2017). Insectageddon: farming is more and bees effective pollinators of oilseed rape catastrophic than climate breakdown | George (Brassica napus L.). Basic and Applied Ecology, Vol Monbiot. The Guardian. 32, 66–76. 25. Carrington, D. (2019). Plummeting insect numbers 7. Biesmeijer, J. C. (2006). Parallel Declines in ‘threaten collapse of nature’. The Guardian. Pollinators and Insect-Pollinated Plants in Britain and 26. Sánchez-Bayo, F. et al. (2019). Worldwide decline of the Netherlands. Science, Vol 313, 351–354. the entomofauna: A review of its drivers. Biological 8. Bohan, D. A. et al. (2011). National-scale regulation of Conservation, Vol 232, 8–27. the weed seedbank by carabid predators: Carabid 27. Simmons, B. I. et al. (2019). Worldwide insect seed predation. Journal of Applied Ecology, Vol 48, declines: An important message, but interpret with 888–898. caution. Ecology and Evolution, Vol 9, 3678–3680. 9. Macadam, C. R. et al. (2015). More than just fish 28. Komonen, A. et al. (2019). Alarmist by bad design: food: ecosystem services provided by freshwater Strongly popularized unsubstantiated claims insects: Ecosystem services and freshwater insects. undermine credibility of conservation science. Ecological Entomology, Vol 40, 113–123. Rethinking Ecology, Vol 4, 17–19. 10. Rega, C. et al. (2018). A pan-European model of 29. Thomas, C. D. et al. (2019). “Insectageddon”: A call landscape potential to support natural pest control for more robust data and rigorous analyses. Global services. Ecological Indicators, Vol 90, 653–664. Change Biology, Vol 25, 1891–1892. 11. Benton, T. G. et al. (2002). Linking agricultural 30. Wagner, D. L. (2019). Global insect decline: practice to insect and bird populations: a historical Comments on Sánchez-Bayo and Wyckhuys (2019). study over three decades: Farming, insect and bird Biological Conservation, Vol 233, 332–333. populations. Journal of Applied Ecology, Vol 39, 673– 31. Mupepele, A.-C. et al. (2019). Insect decline and its 687. drivers: Unsupported conclusions in a poorly 12. Gilbert, G. et al. (2019). Adverse effects of routine performed meta-analysis on trends—A critique of bovine health treatments containing triclabendazole Sánchez-Bayo and Wyckhuys (2019). Basic and and synthetic pyrethroids on the abundance of Applied Ecology, Vol 37, 20–23. dipteran larvae in bovine faeces. Scientific Reports, 32. Powney, G. D. et al. (2019). Widespread losses of Vol 9, 4315. pollinating insects in Britain. Nature Communications, 13. Morse, D. H. (1971). The Insectivorous Bird as an Vol 10, 1018. Adaptive Strategy. Annual Review of Ecology and 33. Didham, R. K. et al. (2020). Interpreting insect Systematics, Vol 2, 177–200. declines: seven challenges and a way forward. Insect 14. Hallmann, C. A. et al. (2014). Declines in Conservation and Diversity, Vol 13 insectivorous birds are associated with high 34. Thomas, J. A. (2004). Comparative Losses of British neonicotinoid concentrations. Nature, Vol 511, 341. Butterflies, Birds, and Plants and the Global Extinction 15. Mlcek, J. et al. (2014). A Comprehensive Look at the Crisis. Science, Vol 303, 1879–1881. Possibilities of Edible Insects as Food in Europe – A 35. Fox, R. et al. (2014). Long-term changes to the Review. Polish Journal of Food and Nutrition frequency of occurrence of British moths are Sciences, Vol 64, 147–157. consistent with opposing and synergistic effects of 16. Payne, C. L. R. et al. (2016). A systematic review of climate and land-use changes. Journal of Applied nutrient composition data available for twelve Ecology, Vol 51, 949–957. commercially available edible insects, and 36. Hallmann, C. A. et al. (2019). Declining abundance of comparison with reference values. Trends in Food beetles, moths and caddisflies in the Netherlands. Science & Technology, Vol 47, 69–77. Insect Conservation and Diversity, 17. Wickramasinghe, L. P. et al. (2004). Abundance and 37. Warren, M. S. et al. (2001). Rapid responses of Species Richness of Nocturnal Insects on Organic British butterflies to opposing forces of climate and and Conventional Farms: Effects of Agricultural habitat change. Nature, Vol 414, 65–69. Intensification on Bat Foraging. Conservation Biology, 38. Hallmann, C. A. et al. (2019). Declining abundance of Vol 18, 1283–1292. beetles, moths and caddisflies in the Netherlands. 18. Orford, K. A. et al. (2015). The forgotten flies: the Insect Conservation and Diversity importance of non-syrphid Diptera as pollinators. 39. Kunin, W. E. (2019). Robust evidence of declines in Proceedings of the Royal Society B: Biological insect abundance and biodiversity. Nature, Vol 574, Sciences, Vol 282, 20142934. 641–642. 19. Hayhow, D. et al. (2019). The State of Nature 2019. 40. Montgomery, G. A. et al. (2020). Is the insect The State of Nature partnership. apocalypse upon us? How to find out. Biological Conservation, Vol 241, 108327.

POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 6

41. Potts, S. G. et al. (2016). Safeguarding pollinators Smartphone Biodiversity Monitoring. Journal of and their values to human well-being. Nature, Vol Artificial Intelligence Research, Vol 51, 805–827. 540, 220–229. 62. BioDAR. BioDAR. 42. Losey, J. E. et al. (2006). The Economic Value of 63. BioDAR: Grants on the Web. Ecological Services Provided by Insects. BioScience, 64. Bell, J. R. et al. (2013). Predicting Insect Migration Vol 56, 311. Density and Speed in the Daytime Convective 43. Ollerton, J. et al. (2016). Insect pollinators boost the Boundary Layer. PLoS ONE, Vol 8, e54202. market price of culturally important crops: holly, 65. Sutherland, W. J. et al. (2016). A Horizon Scan of mistletoe and the spirit of Christmas. Journal of Global Conservation Issues for 2016. Trends in Pollination Ecology, Vol 19, 93–97. Ecology & Evolution, Vol 31, 44–53. 44. Potts, S. G. et al. (2016). The assessment report on 66. Gill, R. J. et al. (2016). Protecting an Ecosystem pollinators, pollination and food production: summary Service: approaches to understanding and mitigating for policymakers. threats to wild insect pollinators. in Advances in 45. Oliver, T. H. et al. (2015). Declining resilience of Ecological Research. Vol 54, 135–206. Elsevier. ecosystem functions under biodiversity loss. Nature 67. Dincă, V. et al. (2011). Complete DNA barcode Communications, Vol 6, reference library for a country’s butterfly fauna reveals 46. Zhang, H. et al. (2018). Economic valuation of natural high performance for temperate Europe. Proceedings pest control of the summer grain aphid in wheat in of the Royal Society B: Biological Sciences, Vol 278, South East England. Ecosystem Services, Vol 30, 347–355. 149–157. 68. Digital collections programme, Natural History 47. Steele, D. J. et al. (2019). Management and drivers of Museum. change of pollinating insects and pollination services. 69. Pinned Insect Digitisation, Natural History Museum. National Pollinator Strategy: for bees and other 70. Schmidt, S. et al. (2015). DNA barcoding largely pollinators in England, Evidence statements and supports 250 years of classical taxonomy: Summary of Evidence. Defra. identifications for Central European bees 48. Breeze, T. D. et al. (2016). Economic Measures of (Hymenoptera, Apoidea partim ). Molecular Ecology Pollination Services: Shortcomings and Future Resources, Vol 15, 985–1000. Directions. Trends in Ecology & Evolution, Vol 31, 71. Hebert, P. D. N. et al. (2013). A DNA ‘Barcode Blitz’: 927–939. Rapid Digitization and Sequencing of a Natural 49. Beynon, S. A. et al. (2015). The application of an History Collection. PLoS ONE, Vol 8, e68535. ecosystem services framework to estimate the 72. Timmermans, M. J. T. N. et al. (2016). Rapid economic value of dung beetles to the U.K. cattle assembly of taxonomically validated mitochondrial industry: Economic benefits of dung beetles. genomes from historical insect collections. Biological Ecological Entomology, Vol 40, 124–135. Journal of the Linnean Society, Vol 117, 83–95. 50. Lövei, G. L. et al. (1996). Ecology and Behavior of 73. Environmental Change Network. Ground Beetles (Coleoptera: Carabidae). Annual 74. Harvey, D. J. et al. (2011). The stag beetle: a Review of Entomology, Vol 41, 231–256. collaborative conservation study across Europe: Stag 51. Vickery, J. A. et al. (2001). The management of beetle conservation. Insect Conservation and lowland neutral grasslands in Britain: effects of Diversity, Vol 4, 2–3. agricultural practices on birds and their food 75. The Insect Survey, Rothamsted Research. resources. Journal of Applied Ecology, Vol 38, 647– 76. UK Pollinator Monitoring Scheme (PoMS): UK 664. Pollinator Monitoring and Research Partnership. 52. (2018). The Riverfly Census. Salmon & Trout Centre for Ecology & Hydrology. Conservation. 77. Carvalheiro, L. G. et al. (2013). Species richness 53. Salado, R. et al. A survey of freshwater angling in declines and biotic homogenisation have slowed England. Phase 1: angling activity, expenditure and down for NW-European pollinators and plants. economic impact. Environment Agency. Ecology Letters, Vol 16, 870–878. 54. Sumner, S. et al. (2018). Why we love bees and hate 78. Leather, S. R. et al. (2010). Do shifting baselines in wasps: Why we love bees and hate wasps. Ecological natural history knowledge threaten the environment? Entomology, Vol 43, 836–845. The Environmentalist, Vol 30, 1–2. 55. Mwebaze, P. et al. (2018). Measuring public 79. Macgregor, C. J. et al. (2019). Moth biomass perception and preferences for ecosystem services: A increases and decreases over 50 years in Britain. case study of bee pollination in the UK. Land Use Nature Ecology & Evolution, Vol 3, 1645–1649. Policy, Vol 71, 355–362. 80. Basset, Y. et al. (2019). Toward a world that values 56. Saunders, M. E. et al. (2019). Understanding the insects. Science, Vol 364, 1230–1231. evidence informing the insect apocalypse myth. 81. Wider Countryside Butterfly Survey. 57. Pocock, M. J. O. et al. (2015). The Biological Records 82. Brereton, T. M. et al. (2011). Developing and Centre: a pioneer of citizen science. Biological launching a wider countryside butterfly survey across Journal of the Linnean Society, Vol 115, 475–493. the United Kingdom. Journal of Insect Conservation, 58. (2019). Christopher Hassall, Personal Comms. Vol 15, 279–290. 59. Aide, T. M. et al. (2013). Real-time bioacoustics 83. Outhwaite, C. et al. (2019). Annual estimates of monitoring and automated species identification. occupancy for bryophytes, lichens and invertebrates PeerJ, Vol 1, e103. in the UK, 1970 – 2015. Scientific Data., 60. Miller-Struttmann, N. E. et al. (2017). Flight of the 84. Mason, S. C. et al. (2015). Geographical range bumble bee: Buzzes predict pollination services. margins of many taxonomic groups continue to shift PLOS ONE, Vol 12, e0179273. polewards. Biological Journal of the Linnean Society, 61. Zilli, D. et al. (2014). A Hidden Markov Model-Based Vol 115, 586–597. Acoustic Cicada Detector for Crowdsourced 85. Woodcock, B. A. et al. (2019). Meta-analysis reveals that pollinator functional diversity and abundance

POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 7

enhance crop pollination and yield. Nature 108. Ollerton, J. et al. (2014). Extinctions of aculeate Communications, Vol 10, 1481. pollinators in Britain and the role of large-scale 86. Winfree, R. et al. (2015). Abundance of common agricultural changes. Science, Vol 346, 1360–1362. species, not species richness, drives delivery of a 109. Warren, M. S. et al. (2011). A new red list of British real-world ecosystem service. Ecology Letters, Vol butterflies. Insect Conservation and Diversity, 159- 18, 626–635. 172. 87. Pérez‐Méndez, N. et al. (2020). The economic cost of 110. Population trends of UK butterfly species to 2018: losing native pollinator species for orchard production. Official Statistics briefing. Butterfly Conservation. Journal of Applied Ecology, 111. Brereton, T. M. et al. (2018). United Kingdom Butterfly 88. Larsen, S. et al. (2018). Lifting the veil: richness Monitoring Scheme report for 2017. Centre for measurements fail to detect systematic biodiversity Ecology & Hydrology, Butterfly Conservation, British change over three decades. Ecology, Vol 99, 1316– Trust for Ornithology and Joint Nature Conservation 1326. Committee. 89. Outhwaite, C. L. et al. (2018). Prior specification in 112. Bell, J. R. et al. (2015). Long-term phenological Bayesian occupancy modelling improves analysis of trends, species accumulation rates, aphid traits and species occurrence data. Ecological Indicators, Vol climate: five decades of change in migrating aphids. 93, 333–343. Journal of Animal Ecology, Vol 84, 21–34. 90. Isaac, N. J. B. et al. (2015). Bias and information in 113. Bell, J.R., Blumgart, D. & Shortall, C.R. (2020) Are biological records: Bias and information in biological insects declining and at what rate? An analysis of records. Biological Journal of the Linnean Society, Vol standardised, systematic catches of aphid and moth 115, 522–531. abundances across Great Britain. Insect Conservation 91. Identification Trainers for the Future, Natural History and Diversity, 13, doi: 10.1111/icad.12412 Museum. 114. Crop Monitor. 92. Courses and Experiences, Field Studies Council. 115. Growers fear for the future of oilseed rape in the UK 93. Record any species on the go. iRecord App. after latest report. Farmers Guardian. 94. Apprenticeships, Bee Farmers Association. 116. Bélanger, J. et al. (2019). The State of the World’s 95. Godfray, H. C. J. (2002). Challenges for taxonomy. Biodiversity for Food and Agriculture. in FAO Nature, Vol 417, 17–19. Commission on Genetic Resources for Food and 96. Mallet, J. et al. (2003). Taxonomy: renaissance or Agriculture Assessments. 572. Tower of Babel? Trends in Ecology & Evolution, Vol 117. The Insecticide Resistance Action Group (IRAG), 18, 57–59. Agriculture and Horticulture Development Board 97. BioLinks, Field Studies Council. (AHDB). 98. Natural England (2019). Personal Comms. 118. Cannon, R. J. C. (1998). The implications of predicted 99. Shortall, C. R. et al. (2009). Long-term changes in the climate change for insect pests in the UK, with abundance of flying insects. Insect Conservation and emphasis on non-indigenous species. Global Change Diversity, Vol 2, 251–260. Biology, Vol 4, 785–796. 100. Conrad, K. F. et al. (2006). Rapid declines of 119. Vanbergen, A. J. et al. (2018). Risks to pollinators and common, widespread British moths provide evidence pollination from invasive alien species. Nat Ecol Evol, of an insect biodiversity crisis. Biological Vol 2, 16–25. Conservation, Vol 132, 279–291. 120. Roy, H. E. et al. (2012). Invasive alien predator 101. Outhwaite, C. et al. (in review). Complexity of causes rapid declines of native European ladybirds: biodiversity change revealed through long-term trends Alien predator causes declines of native ladybirds. of invertebrates, bryophytes and lichens. Nature Diversity and Distributions, Vol 18, 717–725. Ecology & Evolution, 121. Brown, P. M. J. et al. (2018). Native ladybird decline 102. Brooks, D. R. et al. (2012). Large carabid beetle caused by the invasive harlequin ladybird Harmonia declines in a United Kingdom monitoring network axyridis : evidence from a long-term field study. Insect increases evidence for a widespread loss in insect Conservation and Diversity, Vol 11, 230–239. biodiversity. Journal of Applied Ecology, Vol 49, 122. Zhang, E. et al. (2015). The neonicotinoid 1009–1019. imidacloprid impairs honey bee aversive learning of 103. Knowler, J. . et al. (2016). Trichoptera (Caddisflies) simulated predation. Journal of Experimental Biology, caught by the Rothamsted light trap at Rowardennan, Vol 218, 3199–3205. loch Lomondside throughout 2009. The Glasgow 123. Tan, K. et al. (2014). Imidacloprid Alters Foraging and Naturalist, pp.35-42. Decreases Bee Avoidance of Predators. PLoS ONE, 104. Clausnitzer, V. et al. (2009). Odonata enter the Vol 9, e102725. biodiversity crisis debate: The first global assessment 124. UK Plant Health Risk Register. of an insect group. Biological Conservation, Vol 142, 125. Powney, G. D. et al. (2015). Trait correlates of 1864–1869. distribution trends in the Odonata of Britain and 105. MacGregor, C. J. et al. (2019). Moth biomass Ireland. PeerJ, Vol 3, e1410. increases and decreases over 50 years in Britain. 126. Isaac, N. J. B. (2016). Provision of Evidence Nature Ecology and Evolution, Statements to accompany the UK and England 106. Scheper, J. et al. (2013). Environmental factors Species Trend Indicators and an Overview of the driving the effectiveness of European agri- Causes of Biodiversity Change. Final Report. environmental measures in mitigating pollinator loss - 127 Bonebrake, T. C. et al. (2010). Population decline a meta-analysis. Ecology Letters, Vol 16, 912–920. assessment, historical baselines, and conservation: 107. Woodcock, B. A. et al. (2016). Impacts of Inferring population declines. Conservation Letters, neonicotinoid use on long-term population changes in Vol 3, 371–378 wild bees in England. Nature Communications, Vol 7, 128. Goulson, D. et al. (2015). Bee declines driven by 12459. combined stress from parasites, pesticides, and lack of flowers. Science, Vol 347, 1255957–1255957.

POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 8

129. Senapathi, D. et al. (2017). Landscape impacts on fields. Proceedings of the National Academy of pollinator communities in temperate systems: Sciences, Vol 113, 7261–7265. evidence and knowledge gaps. Functional Ecology, 150. Wan, G. et al. (2014). Bio-effects of near-zero Vol 31, 26–37. magnetic fields on the growth, development and 130. Park, M. G. et al. (2015). Negative effects of reproduction of small brown , Laodelphax pesticides on wild bee communities can be buffered striatellus and brown planthopper, Nilaparvata lugens. by landscape context. Proceedings of the Royal Journal of Insect Physiology, Vol 68, 7–15. Society B: Biological Sciences, Vol 282, 20150299. 151. Lázaro, A. et al. (2016). Electromagnetic radiation of 131. Platts, P. J. et al. (2019). Habitat availability explains mobile telecommunication antennas affects the variation in climate-driven range shifts across multiple abundance and composition of wild pollinators. taxonomic groups. Scientific Reports, Vol 9, 1–10. Journal of Insect Conservation, Vol 20, 315–324. 132. Auffret, A. G. et al. (2019). Synergistic and 152. Baldock, K. C. R. et al. (2015). Where is the UK’s antagonistic effects of land use and non‐native pollinator biodiversity? The importance of urban areas species on community responses to climate change. for flower-visiting insects. Proceedings of the Royal Global Change Biology, Society B: Biological Sciences, Vol 282, 20142849. 133. Potts, S. G. et al. (2010). Declines of managed honey 153. Hill, M. J. et al. (2017). Urban ponds as an aquatic bees and beekeepers in Europe. Journal of biodiversity resource in modified landscapes. Global Apicultural Research, Vol 49, 15–22. Change Biology, Vol 23, 986–999. 134. Gray, A. et al. (2019). Loss rates of honey bee 154. Hill, M. J. et al. (2018). Community heterogeneity of colonies during winter 2017/18 in 36 countries aquatic macroinvertebrates in urban ponds at a multi- participating in the COLOSS survey, including effects city scale. Landscape Ecology, Vol 33, 389–405. of forage sources. Journal of Apicultural Research, 155. Samuelson, A. E. et al. (2018). Lower bumblebee Vol 58, 479–485. colony reproductive success in agricultural compared 135. Motta, E. V. S. et al. (2018). Glyphosate perturbs the with urban environments. Proceedings of the Royal gut microbiota of honey bees. Proceedings of the Society B: Biological Sciences, Vol 285, 20180807. National Academy of Sciences, Vol 115, 10305– 156. Osborne, J. L. et al. (2007). Quantifying and 10310. comparing bumblebee nest densities in gardens and 136. Baude, M. et al. (2016). Historical nectar assessment countryside habitats: Bumblebee nest survey in reveals the fall and rise of floral resources in Britain. gardens and countryside. Journal of Applied Ecology, Nature, Vol 530, 85. Vol 45, 784–792. 137. Lost life: England’s lost and threatened species 157. Goulson, D. et al. (2010). Effects of land use at a (NE233)(Part 3). Natural England. landscape scale on bumblebee nest density and 138. Lawton, J. . et al. (2010). Making Space for Nature: a survival: Landscape effects on bumblebee nest review of England’s wildlife sites and ecological survival. Journal of Applied Ecology, Vol 47, 1207– network. Defra. 1215. 139. Robins, J. et al. (2013). The state of brownfields in the 158. Stelzer, R. J. et al. (2010). Winter Active Bumblebees Thames Gateway. Buglife. (Bombus terrestris) Achieve High Foraging Rates in 140. Owens, A. C. S. et al. (2019). Light pollution is a Urban Britain. PLoS ONE, Vol 5, e9559. driver of insect declines. Biological Conservation, 159. Hanley, M. E. et al. (2015). On the verge? Preferential 108259. use of road-facing hedgerow margins by bumblebees 141. Vanbergen, A. J. et al. (2019). Risk to pollinators from in agro-ecosystems. Journal of Insect Conservation, anthropogenic electro-magnetic radiation (EMR): Vol 19, 67–74. Evidence and knowledge gaps. Science of The Total 160. Baldock, K. C. R. et al. (2019). A systems approach Environment, Vol 695, 133833. reveals urban pollinator hotspots and conservation 142. Knop, E. et al. (2017). Artificial light at night as a new opportunities. Nature Ecology & Evolution, Vol 3, threat to pollination. Nature, Vol 548, 206–209. 363–373. 143. Macgregor, C. J. et al. (2017). The dark side of street 161. Kovács-Hostyánszki, A. et al. (2017). Ecological lighting: impacts on moths and evidence for the intensification to mitigate impacts of conventional disruption of nocturnal pollen transport. Global intensive land use on pollinators and pollination. Change Biology, Vol 23, 697–707. Ecology Letters, Vol 20, 673–689. 144. Shepherd, S. et al. (2018). Extremely Low Frequency 162. Ewald, J. A. et al. (2015). Influences of extreme Electromagnetic Fields impair the Cognitive and weather, climate and pesticide use on invertebrates in Motor Abilities of Honey Bees. Scientific Reports, Vol cereal fields over 42 years. Global Change Biology, 8, Vol 21, 3931–3950. 145. Girling, R. D. et al. (2013). Diesel exhaust rapidly 163. Carvell, C. et al. (2006). Declines in forage availability degrades floral odours used by honeybees. Scientific for bumblebees at a national scale. Biological Reports, Vol 3, 2779. Conservation, Vol 132, 481–489. 146. Vaughan, I. P. et al. (2012). Large-scale, long-term 164. Raine, N. E. et al. (2015). Tasteless pesticides affect trends in British river macroinvertebrates. Global bees in the field. Nature, Vol 521, 38–39. Change Biology, Vol 18, 2184–2194. 165. Holzschuh, A. et al. (2016). Mass-flowering crops 147. Farré-Armengol, G. et al. (2016). Ozone degrades dilute pollinator abundance in agricultural landscapes floral scent and reduces pollinator attraction to across Europe. Ecology Letters, Vol 19, 1228–1236. flowers. New Phytologist, Vol 209, 152–160. 166. Marini, L. et al. (2014). Contrasting effects of habitat 148. Sutherland, W. J. et al. (2018). A 2018 Horizon Scan area and connectivity on evenness of pollinator of Emerging Issues for Global Conservation and communities. Ecography, Vol 37, 544–551. Biological Diversity. Trends in Ecology & Evolution, 167. Vanbergen, A. J. et al. (2014). Status and value of Vol 33, 47–58. pollinators and pollination services. Department for 149. Sutton, G. P. et al. (2016). Mechanosensory hairs in the Environment, Food and Rural Affairs. bumblebees ( Bombus terrestris ) detect weak electric

POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 9

168. Botías, C. et al. (2017). Quantifying exposure of wild 187. Hoopingarner, R. et al. (1991). The costs of bumblebees to mixtures of agrochemicals in beekeeping. II: Survey of Sideline Beekeepers. agricultural and urban landscapes. Environmental American Bee Journal, Vol 131, 114–115. Pollution, Vol 222, 73–82. 188. Breeze, T. D. et al. (2019). Linking farmer and 169. Gill, R. J. et al. (2012). Combined pesticide exposure beekeeper preferences with ecological knowledge to severely affects individual- and colony-level traits in improve crop pollination. People and Nature, Vol 1, bees. Nature, Vol 491, 105. 562–572. 170. Tsvetkov, N. et al. (2017). Chronic exposure to 189. Stokstad, E. (2007). The Case of the Empty Hives. neonicotinoids reduces honey bee health near corn Science, Vol 316, 970–972. crops. Science, Vol 356, 1395–1397. 190. Jacques, A. et al. (2017). A pan-European 171. Nicholls, E. et al. (2018). Monitoring Neonicotinoid epidemiological study reveals honey bee colony Exposure for Bees in Rural and Peri-urban Areas of survival depends on beekeeper education and the U.K. during the Transition from Pre- to Post- disease control. PLOS ONE, Vol 12, e0172591. moratorium. Environ. Sci. Technol., Vol 52, 9391– 191. Fürst, M. A. et al. (2014). Disease associations 9402. between honeybees and bumblebees as a threat to 172. Shardlow, M. (2017). Neonicotinoid Insecticides in wild pollinators. Nature, Vol 506, 364. British Freshwaters: 2016 Water Framework Directive 192. McMahon, D. P. et al. (2015). A sting in the spit: Watch List Monitoring Results and widespread cross-infection of multiple RNA viruses Recommendations. Buglife. across wild and managed bees. Journal of Animal 173. Woodcock, B. A. et al. (2017). Country-specific effects Ecology, Vol 84, 615–624. of neonicotinoid pesticides on honey bees and wild 193. Graystock, P. et al. (2013). The Trojan hives: bees. Science, Vol 356, 1393–1395. pollinator pathogens, imported and distributed in 174. Siviter, H. et al. (2018). Quantifying the impact of bumblebee colonies. Journal of Applied Ecology, pesticides on learning and memory in bees. Journal of 194. Graystock, P. et al. (2013). Emerging dangers: Applied Ecology, Vol 55, 2812–2821. Deadly effects of an emergent parasite in a new 175. Huang, W.-F. et al. (2013). Nosema ceranae Escapes pollinator host. Journal of Invertebrate Pathology, Vol Fumagillin Control in Honey Bees. PLoS Pathogens, 114, 114–119. Vol 9, e1003185. 195. Radzevičiūtė, R. et al. (2017). Replication of honey 176. Mao, W. et al. (2017). Disruption of quercetin bee-associated RNA viruses across multiple bee metabolism by fungicide affects energy production in species in apple orchards of Georgia, Germany and honey bees ( Apis mellifera ). Proceedings of the Kyrgyzstan. Journal of Invertebrate Pathology, Vol National Academy of Sciences, Vol 114, 2538–2543. 146, 14–23. 177. Stanley, D. A. et al. (2015). Neonicotinoid pesticide 196. Bailes, E. J. et al. (2018). First detection of bee exposure impairs crop pollination services provided viruses in hoverfly (syrphid) pollinators. Biology by bumblebees. Nature, Vol 528, 548. Letters, Vol 14, 20180001. 178. Sands, B. et al. (2018). Sustained parasiticide use in 197. Mann, C. M. et al. (2015). Lethal and sub-lethal cattle farming affects dung beetle functional effects of faecal deltamethrin residues on dung- assemblages. Agriculture, Ecosystems & feeding insects. Medical and Veterinary Entomology, Environment, Vol 265, 226–235. Vol 29, 189–195. 179. Wall, R. et al. (2012). Area-wide impact of 198. Van Dijk, T. C. et al. (2013). Macro-Invertebrate macrocyclic lactone parasiticides in cattle dung. Decline in Surface Water Polluted with Imidacloprid. Medical and Veterinary Entomology, Vol 26, 1–8. PLoS ONE, Vol 8, e62374. 180. Smith, D. B. et al. (2019). Developmental exposure to 199. Kurze, S. et al. (2018). Nitrogen enrichment in host pesticide contaminated food impedes bumblebee plants increases the mortality of common Lepidoptera brain growth predisposing adults to become poorer species. Oecologia, Vol 188, 1227–1237. learners. bioRxiv, 200. Martay, B. et al. (2017). Impacts of climate change on 181. Kenna, D. et al. (2019). Pesticide exposure affects national biodiversity population trends. Ecography, flight dynamics and reduces flight endurance in Vol 40, 1139–1151. bumblebees. Ecology and Evolution, Vol 9, 5637– 201. Mair, L. et al. (2014). Abundance changes and habitat 5650. availability drive species’ responses to climate 182. Samuelson, E. E. W. et al. (2016). Effect of acute change. Nature Climate Change, Vol 4, 127. pesticide exposure on bee spatial working memory 202. Kerr, J. T. et al. (2015). Climate change impacts on using an analogue of the radial-arm maze. Scientific bumblebees converge across continents. Science, Reports, Vol 6, Vol 349, 177–180. 183. Arce, A. N. et al. (2017). Impact of controlled 203. Suggitt, A. J. et al. (2019). Widespread Effects of neonicotinoid exposure on bumblebees in a realistic Climate Change on Local Plant Diversity. Current field setting. Journal of Applied Ecology, Vol 54, Biology, Vol 29, 2905-2911.e2. 1199–1208. 204. Phillips, B. B. et al. (2018). Drought reduces floral 184. Feest, A. et al. (2014). Nitrogen deposition and the resources for pollinators. Global Change Biology, Vol reduction of butterfly biodiversity quality in the 24, 3226–3235. Netherlands. Ecological Indicators, Vol 39, 115–119. 205. Warm and wet year brings influx of migrants with 185. Beebase, Beekeeping information resource for mixed fortunes for resident species. National Trust. Beekeepers. 206. Oliver, T. H. et al. (2015). Interacting effects of climate 186. Breeze, T. D. et al. (2017). The costs of beekeeping change and habitat fragmentation on drought- for pollination services in the UK – an explorative sensitive butterflies. Nature Climate Change, Vol 5, study. Journal of Apicultural Research, Vol 56, 310– 941–945. 317. 207. Oliver, T. H. et al. (2017). Large extents of intensive land use limit community reorganization during

POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 10

climate warming. Global Change Biology, Vol 23, mayfly nymphs. Environmental Toxicology and 2272–2283. Chemistry, Vol 32, 1096–1100. 208. Soroye, P. et al. (2020). Climate change contributes 226. Raby, M. et al. (2018). Acute toxicity of 6 to widespread declines among bumble bees across neonicotinoid insecticides to freshwater invertebrates: continents. Science, Vol 367, 685–688. Aquatic toxicity of neonicotinoid insecticides. 209. Gardiner, T. et al. (2020). Glowing, glowing, gone? Environmental Toxicology and Chemistry, Vol 37, Monitoring long-term trends in glow-worm numbers in 1430–1445. south-east England. Insect Conservation and 227. Siviter, H. et al. (2018). Sulfoxaflor exposure reduces Diversity, Vol 13 bumblebee reproductive success. Nature, Vol 561, 210. Coleman, P. C. et al. (2014). Cross-generation 109–112. plasticity in cold hardiness is associated with 228. Siviter, H. et al. (2019). No evidence for negative diapause, but not the non-diapause developmental impacts of acute sulfoxaflor exposure on bee olfactory pathway, in the blow fly Calliphora vicina. Journal of conditioning or working memory. PeerJ, Vol 7, e7208. Experimental Biology, Vol 217, 1454–1461. 229. Bohnenblust, E. W. et al. (2016). Effects of the 211. Pozsgai, G. et al. (2018). Phenological changes of the herbicide dicamba on nontarget plants and pollinator most commonly sampled ground beetle (Coleoptera: visitation: Dicamba and pollinator visitation. Carabidae) species in the UK environmental change Environmental Toxicology and Chemistry, Vol 35, network. International Journal of Biometeorology, Vol 144–151. 62, 1063–1074. 230. Brown, M. J. F. et al. (2016). A horizon scan of future 212. Villalobos-Jiménez, G. et al. (2017). Effects of the threats and opportunities for pollinators and urban heat island on the phenology of Odonata in pollination. PeerJ, Vol 4, e2249. London, UK. International Journal of Biometeorology, 231. Butterflies and the Law. Vol 61, 1337–1346. 232. Legal protection for moths. 213. Hodgson, J. A. et al. (2011). Predicting insect 233. Natural Environment and Rural Communities Act phenology across space and time: Predicting Insect 2006. Phenology. Global Change Biology, Vol 17, 1289– 234. National Pollinator Strategy 2014 to 2024: 1300. implementation. GOV.UK. 214. Schenk, M. et al. (2018). Desynchronizations in bee– 235. Harvey, J. A. et al. (2020). International scientists plant interactions cause severe fitness losses in formulate a roadmap for insect conservation and solitary bees. Journal of Animal Ecology, Vol 87, 139– recovery. Nature Ecology & Evolution, 149. 236. Defra (2018). A Green Future: Out 25 Year Plan to 215. Bale, J. S. et al. (2010). Insect overwintering in a Improve the Environment. changing climate. Journal of Experimental Biology, 237. Nature Recovery Network: Discussion Document. Vol 213, 980–994. April 2019. Defra. 216. MacGregor, C. J. et al. (2019). Climate-induced 238. Environment Bill 2019-20 — UK Parliament. phenology shifts linked to range expansions in 239. Bladon, A. J. et al. (2019). Effects of conservation species with multiple reproductive cycles per year. interventions on terrestrial and freshwater Nature Communications, invertebrates: a protocol for subjectwide evidence 217. Thomas, C. (2019). The development of synthesis. Conservation Evidence, Department of Anthropocene biotas. Philosophical Transactions Of Zoology, University of Cambridge. The Royal Society Of London Series B - Biological 240. Tonietto, R. K. et al. (2018). Habitat restoration Sciences, benefits wild bees: A meta-analysis. Journal of 218. Bryden, J. et al. (2013). Chronic sublethal stress Applied Ecology, Vol 55, 582–590. causes bee colony failure. Ecology Letters, Vol 16, 241. Gillingham, P. K. et al. (2015). High Abundances of 1463–1469. Species in Protected Areas in Parts of their 219. Easton, A. H. et al. (2013). The Neonicotinoid Geographic Distributions Colonized during a Recent Insecticide Imidacloprid Repels Pollinating Flies and Period of Climatic Change: Species show higher Beetles at Field-Realistic Concentrations. PLoS ONE, abundance inside PAs. Conservation Letters, Vol 8, Vol 8, e54819. 97–106. 220. Gilburn, A. S. et al. (2015). Are neonicotinoid 242. Thomas, C. D. et al. (2012). Protected areas facilitate insecticides driving declines of widespread species’ range expansions. Proceedings of the butterflies? PeerJ, Vol 3, e1402. National Academy of Sciences, Vol 109, 14063– 221. Whitehorn, P. R. et al. (2018). Larval exposure to the 14068. neonicotinoid imidacloprid impacts adult size in the 243. Nowakowski, M. et al. (2016). Habitat Creation and farmland butterfly Pieris brassicae. PeerJ, Vol 6, Management for Pollinators. e4772. 244. Woodcock, B. A. et al. (2012). Effects of seed addition 222. Woodcock, B. A. et al. (2018). Neonicotinoid residues on beetle assemblages during the re-creation of in UK honey despite European Union moratorium. species-rich lowland hay meadows: Effects of seed PLOS ONE, Vol 13, e0189681. addition on beetle assemblages. Insect Conservation 223. Goulson, D. et al. (2018). Rapid rise in toxic load for and Diversity, Vol 5, 19–26. bees revealed by analysis of pesticide use in Great 245. Pywell, R. F. et al. (2015). Wildlife-friendly farming Britain. PeerJ, Vol 6, e5255. increases crop yield: evidence for ecological 224. Kessler, S. C. et al. (2015). Bees prefer foods intensification. Proceedings of the Royal Society B: containing neonicotinoid pesticides. Nature, Vol 521, Biological Sciences, Vol 282, 20151740. 74. 246. Alison, J. et al. (2017). Successful restoration of moth 225. Roessink, I. et al. (2013). The neonicotinoid abundance and species-richness in grassland created imidacloprid shows high chronic toxicity to mayfly under agri-environment schemes. Biological nymphs: Imidacloprid shows high chronic toxicity to Conservation, Vol 213, 51–58.

POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 11

247. Alison, J. et al. (2016). Spatial targeting of habitat 267. Ksiazek, K. et al. (2012). An assessment of pollen creation has the potential to improve agri-environment limitation on Chicago green roofs. Landscape and scheme outcomes for macro-moths. Journal of Urban Planning, Vol 107, 401–408. Applied Ecology, Vol 53, 1814–1822. 268. Noordijk, J. et al. (2009). Optimizing grassland 248. Important Invertebrate Areas. Buglife. management for flower-visiting insects in roadside 249. Ballantyne, G. et al. (2015). Constructing more verges. Biological Conservation, Vol 142, 2097–2103. informative plant–pollinator networks: visitation and 269. Watson, C. J. et al. (2019). Ecological and economic pollen deposition networks in a heathland plant benefits of low‐intensity urban lawn management. community. Proceedings of the Royal Society B: Journal of Applied Ecology, Biological Sciences, Vol 282, 20151130. 270. Hicks, D. M. et al. (2016). Food for Pollinators: 250. Dicks, L. V. et al. (2010). Bee Conservation: Evidence Quantifying the Nectar and Pollen Resources of for the effects of interventions. Pelagic Publishing. Urban Flower Meadows. PLOS ONE, Vol 11, 251. Sotherton, N. W. (1991). Conservation Headlands: a e0158117. practical combination of intensive cereal farming and 271. Blackmore, L. M. et al. (2014). Evaluating the conservation. in The Ecology of Temperate Cereal effectiveness of wildflower seed mixes for boosting Fields. 373–397. Blackwell Scientific Publications. floral diversity and bumblebee and hoverfly 252. Bennett, A. B. et al. (2014). Landscape composition abundance in urban areas. Insect Conservation and influences pollinators and pollination services in Diversity, Vol 7, 480–484. perennial biofuel plantings. Agriculture, Ecosystems & 272. Salisbury, A. et al. (2019). Enhancing gardens as Environment, Vol 193, 1–8. habitats for soil-surface-active invertebrates: should 253. Carvell, C. et al. (2017). Bumblebee family lineage we plant native or exotic species? Biodiversity and survival is enhanced in high-quality landscapes. Conservation, Nature, Vol 543, 547. 273. Keilsohn, W. et al. (2018). Roadside habitat impacts 254. Tonietto, R. et al. (2011). A comparison of bee insect traffic mortality. Journal of Insect Conservation, communities of Chicago green roofs, parks and Vol 22, 183–188. prairies. Landscape and Urban Planning, Vol 103, 274. Larson, J. L. et al. (2013). Assessing Insecticide 102–108. Hazard to Bumble Bees Foraging on Flowering 255. Senapathi, D. et al. (2015). The impact of over 80 Weeds in Treated Lawns. PLoS ONE, Vol 8, e66375. years of land cover changes on bee and wasp 275. Pesticide-Free Towns, Pesticide Action Network UK. pollinator communities in England. Proceedings of the 276. How it works, Green Flag Award. Royal Society B: Biological Sciences, Vol 282, 277. MacIvor, J. S. et al. (2015). ‘Bee Hotels’ as Tools for 20150294. Native Pollinator Conservation: A Premature Verdict? 256. Batáry, P. et al. (2007). Responses of grassland PLOS ONE, Vol 10, e0122126. specialist and generalist beetles to management and 278. Goulson, D. (2019). The Garden Jungle: or Gardening landscape complexity. Diversity and Distributions, Vol to Save the Planet. Random House. 13, 196–202. 279. Barkham, P. (2018). How to rewild your garden: ditch 257. Van Geert, A. et al. (2010). Do linear landscape chemicals and decorate the concrete. The Guardian. elements in farmland act as biological corridors for 280. Rewilding Britain Fantastic mini-beasts (and how to pollen dispersal?: Linear landscape elements as revive them). Rewilding Britain. corridors. Journal of Ecology, Vol 98, 178–187. 281. Give Nature a Home in Your Garden | Your Personal 258. M’Gonigle, L. K. et al. (2015). Habitat restoration Plan. The RSPB. promotes pollinator persistence and colonization in 282. Wildlife Gardening, The Wildlife Trusts. intensively managed agriculture. Ecological 283. Ricketts, T. H. et al. (2008). Landscape effects on Applications, Vol 25, 1557–1565. crop pollination services: are there general patterns? 259. Agriculture Bill 2019-20 — UK Parliament. Ecology Letters, Vol 11, 499–515. 260. Pe’er, G. et al. (2017). Adding Some Green to the 284. Garibaldi, L. A. et al. (2011). Stability of pollination Greening: Improving the EU’s Ecological Focus Areas services decreases with isolation from natural areas for Biodiversity and Farmers: Evaluation of EU’s despite honey bee visits: Habitat isolation and ecological focus areas. Conservation Letters, Vol 10, pollination stability. Ecology Letters, Vol 14, 1062– 517–530. 1072. 261. Countryside Stewardship. GOV.UK. 285. Kennedy, C. M. et al. (2013). A global quantitative 262. Canvey Wick Nature Reserve, Canvey Island, Essex. synthesis of local and landscape effects on wild bee The RSPB. pollinators in agroecosystems. Ecology Letters, Vol 263. Tarrant, S. et al. (2013). Grassland Restoration on 16, 584–599. Landfill Sites in the East Midlands, United Kingdom: 286. Carvell, C. et al. (2015). Effects of an agri- An Evaluation of Floral Resources and Pollinating environment scheme on bumblebee reproduction at Insects: Flowers and Pollinating Insects on Restored local and landscape scales. Basic and Applied Landfills. Restoration Ecology, Vol 21, 560–568. Ecology, Vol 16, 519–530. 264. Moroń, D. et al. (2014). Railway Embankments as 287. Wood, T. J. et al. (2015). Pollinator-friendly New Habitat for Pollinators in an Agricultural management does not increase the diversity of Landscape. PLoS ONE, Vol 9, e101297. farmland bees and wasps. Biological Conservation, 265. Garbuzov, M. et al. (2014). Listmania: The Strengths Vol 187, 120–126. and Weaknesses of Lists of Garden Plants to Help 288. McCracken, M. E. et al. (2015). Social and ecological Pollinators. BioScience, Vol 64, 1019–1026. drivers of success in agri-environment schemes: the 266. Garbuzov, M. et al. (2014). Quantifying variation roles of farmers and environmental context. Journal of among garden plants in attractiveness to bees and Applied Ecology, Vol 52, 696–705. other flower-visiting insects. Functional Ecology, Vol 289. ASSIST, Achieving Sustainable Agricultural Systems. 28, 364–374. 290. The Cool Farm Tool.

POSTNOTE 619 March 2020 UK Insect Decline and Extinctions Page 12

291. Estay, S. A. et al. (2012). Increased outbreak frequency associated with changes in the dynamic behaviour of populations of two aphid species. Oikos, Vol 121, 614–622. 292. Southwood, T. R. E. (1961). The Number of Species of Insect Associated with Various Trees. The Journal of Animal Ecology, Vol 30, 1. 293. Kennedy, C. E. J. et al. (1984). The Number of Species of Insects Associated with British Trees: A Re-Analysis. The Journal of Animal Ecology, Vol 53, 455. 294. Alexander, K. et al. (2006). The value of different tree and shrub species to wildlife. British Wildlife, Vol 18, 18. 295. Woodland Trust British trees to plant in your garden: 14 native tree ideas. Woodland Trust. 296. Woodland Trust A-Z Guide - British Trees. Woodland Trust. 297. The value of different tree species for insects and lichens. 298. Hodgson, J. A. et al. (2010). Comparing organic farming and land sparing: optimizing yield and butterfly populations at a landscape scale: Organic farming and land sparing. Ecology Letters, Vol 13, 1358–1367. 299. Create beetle banks. Conservation Evidence, Department of Zoology, University of Cambridge. 300. Dicks, L. V. et al. (2014). Farmland Conservation: Evidence for the effects of interventions in northern and western Europe. Pelagic Publishing Ltd. 301. Dicks, L. V. et al. (2016). Ten policies for pollinators. Science, Vol 354, 975–976. 302. Natural Pest Control, Conservation Evidence: Department of Zoology, University of Cambridge 303. Integrated Pest Management, NFU. Voluntary Initiative. 304. Integrated Pest Management. Voluntary Initiative. 305. Willis, S. G. et al. (2009). Assisted colonization in a changing climate: a test-study using two U.K. butterflies. Conservation Letters, Vol 2, 46–52. 306. International Union for Conservation of Nature and Natural Resources et al. (2013). Guidelines for reintroductions and other conservation translocations. 307. Large Blue Butterfly Collaborating to conserve. Centre for Ecology & Hydrology. 308. Fox, R. et al. (2015). The State of the UK’s Butterflies 2015. Butterfly Conservation and the Centre for Ecology & Hydrology,. 309. Thomas, J. A. et al. (2009). Successful Conservation of a Threatened Maculinea Butterfly. Science, Vol 325, 80–83.